Taxonomy, distribution and biology of lettuce powdery mildew (Golovinomyces cichoracearum sensu stricto)

This paper reviews the taxonomy, biology, importance, host–pathogen interactions and control of lettuce powdery mildew. The main causal agent of this disease, Golovinomyces cichoracearum s.s., is an important powdery mildew pathogen of many members of the family Asteraceae. The pathogen is distributed worldwide and occurs on Lactuca sativa as well as wild Lactuca spp. and related taxa (e.g. Cichorium spp.). Powdery mildew of lettuce can be a major problem in production areas with favourable environmental conditions for disease development (dry, hot weather). The fungus grows ectophytically and appears as white, powdery growth on both the upper and lower sides of leaves. There is rather limited information on the geographic distribution of powdery mildew on wild Lactuca spp. Most L. sativa cultivars have been found to be susceptible. Large variability in virulence was confirmed and existence of different races is supposed. Resistance in L. sativa and some related wild Lactuca spp. is characterized by race-specificity, but the genetic background of resistance is poorly understood. Sources of resistance are known in L. saligna and L. virosa. Lettuce powdery mildew can be effectively controlled by common fungicides (e.g. sulphur, myclobutanil, quinoline, strobilurins, etc.) and protective compounds (e.g. extract of neem oil, Reynoutria sachaliensis extracts). However, fungicide resistance may arise. Non-fungicidal activators of plant systemic acquired resistance (SAR) had no direct effect on the causal agent. Future issues regarding lettuce powdery mildew research are summarized.

[1]  U. Braun Some critical notes on the classification and the generic concept of the Erysiphaeeae , 2013 .

[2]  A. Lebeda,et al.  North American Continent - a New Source of Wild Lactuca spp. Germplasm Variability for Future Lettuce Breeding , 2011 .

[3]  R. Niks,et al.  Genetic dissection of Lactuca saligna nonhost resistance to downy mildew at various lettuce developmental stages , 2009 .

[4]  U. Braun,et al.  Conidial germination patterns in powdery mildews. , 2009, Mycological research.

[5]  A. Lebeda,et al.  Wild Lactuca germplasm for lettuce breeding: current status, gaps and challenges , 2009, Euphytica.

[6]  V. Funk Systematics, evolution, and biogeography of Compositae , 2009 .

[7]  D. Glawe,et al.  The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. , 2008, Annual review of phytopathology.

[8]  A. Lebeda,et al.  Diversity of defence mechanisms in plant–oomycete interactions: a case study of Lactuca spp. and Bremia lactucae , 2008, European Journal of Plant Pathology.

[9]  A. Lebeda,et al.  Structure and variation in the wild-plant pathosystem: Lactuca serriola–Bremia lactucae , 2008, European Journal of Plant Pathology.

[10]  S. Takamatsu,et al.  Molecular phylogeny and evolution of the genus Neoerysiphe (Erysiphaceae, Ascomycota). , 2008, Mycological research.

[11]  C. Chupp,et al.  Vegetable diseases and their control , 2008, American Potato Journal.

[12]  A. Newton,et al.  Induced Resistance in Natural Ecosystems and Pathogen Population Biology: Exploiting Interactions , 2007 .

[13]  H. Jee,et al.  First report of powdery mildew caused by Podosphaera fusca on Lactuca sativa in Korea , 2006 .

[14]  P. E. Russell,et al.  FRAC: combined resistance risk assessment , 2006 .

[15]  Ale Lebeda,et al.  Lettuce (Asteraceae; Lactuca spp.) , 2006 .

[16]  S. Takamatsu,et al.  Molecular phylogeny supports a Northern Hemisphere origin of Golovinomyces (Ascomycota: Erysiphales). , 2006, Mycological research.

[17]  K. Garrett,et al.  Climate change effects on plant disease: genomes to ecosystems. , 2006, Annual review of phytopathology.

[18]  H. Lot,et al.  A Color Atlas of Diseases of Lettuce and Related Salad Crops: Observation, Biology and Control , 2006 .

[19]  S. Koike,et al.  Vegetable Diseases: A Colour Handbook , 2006 .

[20]  S. Trdan,et al.  Efficacy of Three Natural Chemicals to Reduce the Damage of Erysiphe cichoracearum on Chicory in Two Meteorologically Different Growing Seasons , 2004 .

[21]  A. Lebeda,et al.  Occurrence of Bremia lactucae in Natural Populations of Lactuca serriola , 2004 .

[22]  S. Takamatsu Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences , 2004 .

[23]  H. Su,et al.  Sporulation of Bremia lactucae Affected by Temperature, Relative Humidity, and Wind in Controlled Conditions. , 2004, Phytopathology.

[24]  A. Lebeda,et al.  Biodiversity and ecogeography of wild Lactuca spp. in some European countries , 2001, Genetic Resources and Crop Evolution.

[25]  A. Lebeda Differences in resistance of wild Lactuca species to natural infection of lettuce powdery mildew (Erysiphe cichoracearum) , 1985, Euphytica.

[26]  A. Lebeda Evaluation of wild Lactuca species for resistance of natural infection of powdery mildew (Erysiphe cichoracearum) , 2004, Genetic Resources and Crop Evolution.

[27]  M. Matheron,et al.  Evaluation of Lettuce Cultivar Susceptibility to Powdery Mildew in 2003 , 2003 .

[28]  A. Lebeda,et al.  Characterization of New Highly Virulent German Isolates of Bremia lactucae and Efficiency of Resistance in Wild Lactuca spp. Germplasm , 2003 .

[29]  S. Takamatsu,et al.  Evolution of host-parasite relationships of Golovinomyces (Ascomycete: Erysiphaceae) inferred from nuclear rDNA sequences. , 2003, Molecular phylogenetics and evolution.

[30]  R. Kennedy,et al.  Comparative morphological studies on tomato powdery mildew (Oidium neolycopersici) , 2002 .

[31]  A. Lebeda,et al.  Occurrence of powdery mildew on Lactuca viminea subsp. Chondrilliflora in south France. , 2002 .

[32]  Uwe Braun,et al.  The taxonomy of the powdery mildew fungi. , 2002 .

[33]  A. Lebeda,et al.  Aspects of the Interactions between Wild Lactuca Spp. and Related Genera and Lettuce Downy Mildew (Bremia Lactucae) , 2002 .

[34]  M. Matheron,et al.  Reaction of Different Cultivars of Lettuce to Development of Powdery Mildew on Lettuce in 2001 , 2001 .

[35]  M. McGrath Fungicide Resistance in Cucurbit Powdery Mildew: Experiences and Challenges. , 2001, Plant disease.

[36]  S. Takamatsu,et al.  Molecular phylogeny and radiation time of Erysiphales inferred from the nuclear ribosomal DNA sequences , 2000 .

[37]  Shin HyeonDong Erysiphaceae of Korea. , 2000 .

[38]  S. Takamatsu,et al.  Evolutionary analysis of the powdery mildew fungi using nucleotide sequences of the nuclear ribosomal DNA. , 2000 .

[39]  U. Braun,et al.  Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rDNA ITS sequences, some taxonomic consequences , 2000 .

[40]  John W. Taylor,et al.  Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. , 1999 .

[41]  S. Takamatsu,et al.  Phylogenetic relationships ofMicrosphaera andErysiphe sectionErysiphe (powdery mildews) inferred from the rDNA ITS sequences , 1999 .

[42]  M. Heil Systemic acquired resistance: available information and open ecological questions , 1999 .

[43]  E. Ryder Lettuce, Endive and Chicory , 1999 .

[44]  S. Takamatsu,et al.  Phylogenetic analysis and predicted secondary structures of the rDNA internal transcribed spacers of the powdery mildew fungi (Erysiphaceae) , 1998 .

[45]  K. Subbarao,et al.  Compendium of Lettuce Diseases , 1997 .

[46]  R. Cook,et al.  Identification and classification of powdery mildew anamorphs using light and scanning electron microscopy and host range data , 1997 .

[47]  M. Akram,et al.  Evaluation of the susceptibility of some lettuce cultivars to natural infection by powdery mildew (Erysiphe cichoracearum) , 1996 .

[48]  S. Koike,et al.  Occurrence of powdery mildew, caused by Erysiphe cichoracearum, on endive and radicchio in California. , 1996 .

[49]  K. Zeller,et al.  Intraspecies differentiation in the powdery mildew Erysiphe cichoracearum determined with rDNA RFLPs , 1995 .

[50]  U. Braun The powdery mildews (Erysiphales) of Europe , 1995 .

[51]  I. Crute,et al.  Resistance to Erysiphe fischeri in two populations of Senecio vulgaris , 1993 .

[52]  K. Amano Host Range and Geographical Distribution of the Powdery Mildew Fungi , 1990 .

[53]  U. Braun A monograph of the Erysiphales (powdery mildews) , 1987 .

[54]  I. Wright,et al.  Resistance of lettuce varieties to powdery mildew , 1986 .

[55]  A. Lebeda,et al.  Occurrence of Erysiphe cichoracearum Perithecia on Wild Lactuca Species , 1986 .

[56]  Dipl.-Landw. Horst Klemm Ein bemerkenswertes Schadauftreten von Echtem Mehltau (Erysiphe cichoracearum DC. ex Mérat) an Kopfsalat (Lactuca sativa L.) in der DDR , 1985 .

[57]  I. Crute,et al.  Powdery mildew of lettuce (Lactuca sativa) , 1983 .

[58]  G. Dixon Vegetable Crop Diseases , 1981, Palgrave Macmillan UK.

[59]  K. Hammett Taxonomy of Erysiphaceae in New Zealand , 1977 .

[60]  J. J. Baker Report on diseases of cultivated plants in England and Wales for the years 1957-1968 , 1974 .

[61]  K. Hirata Host range and geographical distribution of the powdery mildews. , 1966 .

[62]  W. Schnathorst Environmental Relationships in the Powdery Mildews , 1965 .

[63]  W. Schnathorst Relation of microclimates to the development of powdery mildew of Lettuce. , 1960 .

[64]  W. Schnathorst Effects of temperature and moisture stress on the Lettuce powdery mildew fungus. , 1960 .

[65]  W. Schnathorst Heterothallism in the Lettuce Strain of Erysiphe Cichoracearum , 1959 .

[66]  S. Blumer Die Erysiphaceen Mitteleuropas unter besonderer Berucksichtigung der Schweiz , 1933 .